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Title: Walnut consumption alters the gastrointestinal microbiota, microbially derived secondary bile acids, and health markers in healthy adults: a randomized controlled trial

Author
item HOLSCHER, HANNAH - University Of Illinois
item GUETTERMAN, HEATHER - University Of Illinois
item SWANSON, KELLY - University Of Illinois
item AN, R - University Of Illinois
item MATTHAN, NIRUPA - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item LICHTENSTEIN, ALICE - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item Novotny, Janet
item Baer, David

Submitted to: Journal of Nutrition
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2018
Publication Date: 5/3/2018
Citation: Holscher, H.D., Guetterman, H.M., Swanson, K.S., An, R., Matthan, N., Lichtenstein, A., Novotny Dura, J., Baer, D.J. 2018. Walnut consumption alters the gastrointestinal microbiota, microbially derived secondary bile acids, and health markers in healthy adults: a randomized controlled trial. Journal of Nutrition. 148:861-867. https://doi.org/10.1093/jn/nxy004.
DOI: https://doi.org/10.1093/jn/nxy004

Interpretive Summary: Diets that contain nuts have beneficial effects on health. Data from epidemiological studies demonstrate that diets that include nuts are associated with reduce risk of death, especially death from cancer and heart disease. Animal studies also demonstrate that when walnuts are incorporated into the diet, there is a beneficial impact on the gastrointestinal microbiota, and gut and metabolic health. However, these relationships among diet, walnut consumption and gut health have not been investigated in humans. We conducted a controlled feeding study with humans to assess the impact of walnut consumption on the human gastrointestinal microbiota, the gut metabolome, and metabolic markers of health. A controlled-feeding, randomized, crossover study was undertaken in healthy adults. Study participants alternatively received isocaloric treatment diets containing 0 grams or 42 grams/day (0 or 1.5 oz/day) of walnut pieces for two 3-week periods with a 1-week break in-between the two diet periods. Fecal and blood samples were collected before the study started and at the end of each treatment period. Compared to the end of the control (no walnut) period, walnut consumption increased the relative abundance of Faecalibacterium, Clostridium, Dialister, and Roseburia, and reduced the relative abundances of Ruminococcus, Dorea, Oscillospira, and Bifidobacterium. Secondary bile acids (deoxycholic and lithocholic) are produced from bile acids by microbes in the large intestine, and it has been suggested that these compounds may increase risk for colorectal cancer. The concentration of these compounds in the feces was reduced when walnuts were in the diet. Thus, adding walnuts to the diet impacted the composition and function of the human microbiota, increasing Firmicutes in butyrate-producing Clostridium clusters XVIa and IV, including Faecalibacterium and Roseburia, and reducing microbial derived, proinflammatory secondary bile acids. These results suggest the gut microbiota may contribute to the underlying mechanisms of the beneficial health effects of walnut consumption. These data are important to consumers interested in improving their diet quality and reducing their risk for disease, health professionals who provide dietary advice, and scientists interested in the underlying mechanisms of diet and disease.

Technical Abstract: Epidemiologic data suggest that diets rich in nuts have beneficial health effects, including reducing total and cause-specific mortality from cancer and heart disease. Although there is accumulating preclinical evidence that walnuts beneficially affect the gastrointestinal microbiota and gut and metabolic health, these relations have not been investigated in humans. We aimed to assess the impact of walnut consumption on the human gastrointestinal microbiota and metabolic markers of health. A controlled-feeding, randomized crossover study was undertaken in healthy men and women [n = 18; mean age = 53.1 y; body mass index (kg/m2): 28.8]. Study participants received isocaloric diets containing 0 or 42 g walnuts/d for two 3-wk periods, with a 1-wk washout between diet periods. Fecal and blood samples were collected at baseline and at the end of each period to assess secondary outcomes of the study, including effects of walnut consumption on fecal microbiota and bile acids and metabolic markers of health. Compared with after the control period, walnut consumption resulted in a 49-160% higher relative abundance of Faecalibacterium, Clostridium, Dialister, and Roseburia and 16-38% lower relative abundances of Ruminococcus, Dorea, Oscillospira, and Bifidobacterium (P < 0.05). Fecal secondary bile acids, deoxycholic acid and lithocholic acid, were 25% and 45% lower, respectively, after the walnut treatment compared with the control treatment (P < 0.05). Serum LDL cholesterol and the noncholesterol sterol campesterol concentrations were 7% and 6% lower, respectively, after walnut consumption compared with after the control treatment (P < 0.01). Walnut consumption affected the composition and function of the human gastrointestinal microbiota, increasing the relative abundances of Firmicutes species in butyrate-producing Clostridium clusters XIVa and IV, including Faecalibacterium and Roseburia, and reducing microbially derived, proinflammatory secondary bile acids and LDL cholesterol. These results suggest that the gastrointestinal microbiota may contribute to the underlying mechanisms of the beneficial health effects of walnut consumption.